Selective loss and axonal sprouting of GABAergic interneurons in the sclerotic hippocampus induced by LiClPilocarpine

International Journal of Neuroscience

Volumn 121, Issue 2, 2011, Pages 69-85

  Long, Lili ^a   Xiao, Bo ^a   Feng, Li ^a   Yi, Fang ^a   Li, Guoliang ^a   Li, Shuyu ^a   Mutasem, M Abuhamed ^a   Chen, Si ^a   Bi, Fangfang ^a   Li, Yi ^a  

^a CENTRAL SOUTH UNIVERSITY   (China)

Author keywords

Epilepsy; Hippocampus; Neuropeptide Y; Parvalbumin; Somatostatin

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR; FLUORESCENT DYE; LITHIUM CHLORIDE; NEUROPEPTIDE Y; PARVALBUMIN; PILOCARPINE; SOMATOSTATIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BEHAVIOR CHANGE; CELL LOSS; CONTROLLED STUDY; DENDRITE; EPILEPTIC STATE; HIPPOCAMPAL CA1 REGION; HIPPOCAMPAL SCLEROSIS; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; INTERNEURON; MALE; MORTALITY; NERVE CELL DEGENERATION; NERVE SPROUTING; NEUTROPHIL; NISSL STAINING; NONHUMAN; QUANTITATIVE ANALYSIS; RAT; STAINING; TEMPORAL LOBE EPILEPSY;

ANIMALS; AXONS; DISEASE MODELS, ANIMAL; GAMMA-AMINOBUTYRIC ACID; HIPPOCAMPUS; INTERNEURONS; LITHIUM CHLORIDE; MALE; NERVE DEGENERATION; NEUROPEPTIDE Y; PARVALBUMINS; PILOCARPINE; RATS; RATS, SPRAGUE-DAWLEY; SCLEROSIS; SOMATOSTATIN; STATUS EPILEPTICUS;

EID: 78651108981     PISSN: 00207454     EISSN: 15635279     Source Type: Journal    
DOI: 10.3109/00207454.2010.530007     Document Type: Article

References (63)

1. Adnan, H. S., & Shirley, A. J. (2005). CA3 axonal sprouting in kainate-induced chronic epilepsy. Brain Research, 1066, 129-146.
2. Andre, V., Marescaux, C., Nehlig, A., & Fritschy, J. M. (2001). Alterations of hippocampal GABAergic system contribute to development of spontaneous recurrent seizures in the rat lithiumpilocarpine model of temporal lobe epilepsy. Hippocampus, 11, 452-468.
3. Andrioli, A., Alonso-Nanclares, L., Arellano, J. I., & DeFelipe, J. (2007). Quantitative analysis of parvalbumin-immunoreactive cells in the human epileptic hippocampus. Neuroscience, 149, 131-143.
4. Arellano, J. I., Munoz, A., Ballesteros-Yanez, I., Sola, R. G., & DeFilipe, J. (2004). Histopathology and reorganization of chandelier cells in the human epileptic sclerotic hippocampus. Brain, 127, 45-64.
5. Babb, T. L., Brown, W. J., Pretorius, J., Davenport, C., Lieb, J. P., & Crandall, P. H. (1984). Temporal lobe volumetric cell densities in temporal lobe epilepsy. Epilepsia, 25, 729-740.
6. Babb, T. L., Pretorius, J. K., Kupfer, W. R., & Crandall, P. H. (1989). Glutamate decarboxylase-immunoreactive neurons are preserved in human epileptic hippocampus. Journal of Neuroscience, 9, 2562-2574.
7. Bausch, S. B. (2005). Axonal sprouting of GABAergic interneurons in temporal lobe epilepsy. Epilepsy & Behavior, 7, 390-400.
8. Berg, A. T. (2006). Defining intractable epilepsy. Advances in Neurology, 97, 5-10.
9. Bouilleret, V., Ridoux, V., Depaulis, A., Marescaux, C., Nehlig, A., & Le Gal La Salle, G. (1999). Recurrent seizures and hippocampal sclerosis following intrahippocampal kainate injection in adult mice: Electroencephalography, histopathology and synaptic reorganization similar to mesial temporal lobe epilepsy. Neuroscience, 89, 717-729.
10. Buckmaster, P. S., & Dudek, F. E. (1997). Neuron loss, granule cell axon reorganization, and functional changes in the dentate gyrus of epileptic kainate-treated rats. Journal of Comparative Neurology, 385, 385-404.
11. Cascino, G. D. (2005). Temporal lobe epilepsy: More then hippocampal pathology. Epilepsy Currents, 5, 187-189.
12. Cavalheiro, E. A., Silva, D. F., Turski,W. A., Calderazzo-Filho, L. S., Bortolotto, Z. A., & Turski, L. (1987). The susceptibility of rats to pilocarpine-induced seizures is age-dependent. Developmental Brain Research, 37, 43-58.
13. Chen, S., Kobayashi, M., Honda, Y., Kakuta, S., Sato, F., & Kishi, K. (2007). Preferential neuron loss in the rat piriform cortex following pilocarpine-induced status epilepticus. Epilepsy Research, 74, 1-18.
14. Clifford,D. B., Olney, J.W.,Maniotis, A., Collins, R. C., & Zorumski, C. F. (1987). The functional anatomy and pathology of lithiumpilocarpine and high-dose pilocarpine seizures. Neuroscience, 23, 953-968.
15. Cossart, R., Dinocourt, C., Hirsch, J. C., Merchan-Perez, A., De Felipe, J., Ben-Ari, Y., et al. (2001). Dendritic but not somatic GABAergic inhibition is decreased in experimental epilepsy. Nature Neuroscience, 4, 52-62.
16. DeLanerolle, N. C., Brines, M. L., & Kim, J. H. (1992). Neurochemical remodeling of the hippocampus in human temporal lobe epilepsy. In J. Engel, Jr., C.Wasterlain, E. A. Cavalheiro, U. Heinemann & G. Avanzini (eds.), Molecular Biology of Epilepsy. Amsterdam: Elsevier, 205-220.
17. Dichter, M. A., & Wilcox, K. S. (1997). Excitatory synaptic transmission. In J. Engel, Jr. and T. A. Pedley (eds.), Epilepsy: A Comprehensive Textbook. Philadelphia: Lippincott-Raven, 251.
18. Dinocourt, C., Petanjek, Z., Freund, T. F., Ben-Ari, Y., & Esclapez, M. (2003). Loss of interneurons innervating pyramidal cell dendrites and axon initial segments in the CA1 region of the hippocampus following pilocarpine-induced seizures. Journal of Comparative Neurology, 459, 407-425.
19. Doherty, J., & Dingledine, R. (2000). Reduced excitatory drive onto interneurons in the dentate gyrus after status epilepticus. Journal of Neuroscience, 21, 2048-2057.
20. Esclapez, M., & Houser, C. R. (1995). Somatostatin neurons are a subpopulation of GABA neurons in the rat dentate gyrus: Evidence from colocalization of pre-prosomatostatin and glutamate decarboxylase messenger RNAs. Neuroscience, 64, 339-355.
21. Falcomer, M. A. (1974). Mesial temporal (Ammons horn) sclerosis as a common cause of epilepsy. Aetiology, treatment, and prevention. Lancet, 2, 767-770.
22. Falcomer,M. A., Serafetinides, E. A., & Corsellis, J. A. (1964). Etiology and pathogenesis of temporal lobe epilepsy. Archives of Neurology, 10, 233-248.
23. Franck, J. E., Kunkel, D. D., Baskin, D. G., & Schwartzkroin, P. A. (1988). Inhibition in kainate-lesioned hyperexcitable hippocampi: Physiologic, autoradio-graphic and immunocytochemical observations. Journal of Neuroscience, 8, 1991-2002.
24. Franck, J. E., & Schwartzkroin, P. A. (1985). Do kainate-lesioned hippocampi become epileptogenic? Brain Research, 389, 309-313.
25. Freund, T. F., & Buzsaki, G. (1996). Interneurons of the hippocampus. Hippocampus, 6, 347-470.
26. Glien, M., Brandt, C., Potschka, H., Voigt, H., Ebert, U., & Löscher, W. (2001). Repeated low-dose treatment of rats with pilocarpine: Low mortality but high proportion of rats developing epilepsy. Epilepsy Research, 46, 111-119.
27. Hellier, J. L., Patrylo, P. R., Dou, P., Nett, M., Rose, G. M., & Dudek, F. E. (1999). Assessment of inhibition and epileptiform activity in the septal dentate gyrus of freely behaving rats during the first week after kainate treatment. Journal of Neuroscience, 19, 10053-10064.
28. Hogan, R. E., Bucholz, R. D., & Joshi, S. (2003). Hippocampal deformation based shape analysis in epilepsy and unilateral mesial temporal sclerosis. Epilepsia, 44, 8002-8061.
29. Jope, R. S., Morrisett, R. A., & Snead, O. C., III, (1986). Characterization of lithium potentiation of pilocarpine-induced status epilepticus in rats. Experimental Neurology, 91, 471-480.
30. Katsumaru, H., Kosaka, T., Heizmann, C. W., & Hama, K. (1988). Immuno-cytochemical study of GABAergic neurons containing the calcium-binding protein parvalbumin in the rat hippocampus. Experimental Brain Research, 72, 347-362.
31. Klitgaard, H., Matagne, A., Vanneste-Goemaere, J., & Margineanu, D. G. (2002). Pilocarpine-induced epileptogenesis in the rat: Impact of initial duration of status epilepticus on electrophysiological and neuropathological alterations. Epilepsy Research, 51, 93-107.
32. Kobayashi, M., & Buckmaster, P. S. (2003). Reduced inhibition of dentate granule cells in amodel of temporal lobe epilepsy. Journal of Neuroscience, 23, 2440-2452.
33. Kosaka, T., Katsumaru, H., Hama, K., Wu, J. Y., & Heizmann, C. W. (1987). GABAergic neurons containing the Ca2+-binding protein parvalbumin in the rat hippocampus and dentate gyrus. Brain Research, 419, 119-130.
34. Lancaster, B., & Wheal, H. V. (1984). Chronic failure of inhibition of the area CA1 area of the hippocampus following kainic acid lesions of the CA3/CA4 area. Brain Research, 295, 317-324.
35. Lemos, T., & Cavalheiro, E. A. (1995). Suppression of pilocarpineinduced status epilepticus and the late development of epilepsy in rats. Experimental Brain Research, 102, 423-428.
36. Li, W. E., & Nagy, J. I. (2000). Activation of fibres in rat sciatic nerve alters phosphorylation state of connexin-43 at astrocytic gap junctions in spinal cord: Evidence for junction regulation by neuronal-glial interactions. Neuroscience, 97, 113-123.
37. Liu, Z., Nagao, T., Desjardins, G. C., Gloor, P., & Avoli, M. (1994). Quantitative evaluation of neuronal loss in the dorsal hippocampus in rats with long-term pilocarpine seizures. Epilepsy Research, 17, 237-247.
38. Longo, B. M., & Mello, L. E. A. M. (1998). Supragranular mossy fiber sprouting is not necessary for spontaneous seizures in the intrahippocampal kainite model of epilepsy in the rat. Epilepsy Research, 32, 172-182.
39. Macdonald, R. L. (1997). Inhibitory synaptic transmission. In J. Engel, Jr. and T. A. Pedley (eds.), Epilepsy: A Comprehensive Textbook. Philadelphia: Lippincott-Raven, 265-275.
40. Magloczky, Z., & Freund, T. F. (2005). Impaired and repaired inhibitory circuits in the epileptic human hippocampus. Trends in Neurosciences, 28, 334-340.
41. Magloczky, Z.,Wittner, L., Borhegyi, Z., Halasz, P., Vajda, J., Czirjak, S., et al. (2000). Changes in the distribution and connectivity of interneurons in the epileptic human dentate gyrus. Neuroscience, 96, 7-25.
42. Margerison, J. H., & Corsellis, J. A. N. (1966). Epilepsy and the temporal lobes. Brain, 89, 499-530.
43. Park, C., Kang, M., Kang, K., Lee, J., Kim, J., Yoo, J., et al. (2001). Differential changes in neuropeptide Y and nicotinamide adenine dinucleotide phosphate-diaphorase-positive neurons in rat hippocampus after kainic acid-induced seizure. Neuroscience Letters, 298, 49-52.
44. Racine, R. J. (1972).Modification of seizure activity by electrical stimulation IIMotor seizure. Electroencephalography and Clinical Neurophysiology, 32, 781-794.
45. Scharfman, H. E. (2007). The neurobiology of epilepsy. Current Neurology and Neuroscience Reports, 7, 348-354.
46. Schwarzer, C., Williamson, J. M., Lothman, E. W., Vezzani, A., & Sperk, G. (1995). Somatostatin, neuropeptide Y, neurokinen B and cholecystokinin immunoreactivity in two chronic models of temporal lobe epilepsy. Neuroscience, 69, 831-845.
47. Shetty, A. K., Hattiangady, B., & Rao, M. S. (2009). Vulnerability of hippocampal GABA-ergic interneurons to kainate-induced excitotoxic injury during old age. Journal of Cell and Molecular Medicine, 13, 2408-2423.
48. Shetty, A. K., & Turner, D. A. (2001). Glutamic acid decarboxylase- 67-positive hippocampal interneurons undergo a permanent reduction in number following kainic acid-induced degeneration of ca3 pyramidal neurons. Experimental Neurology, 169, 276-297.
49. Sloviter, R. S. (1987). Decreased hippocampal inhibition and a selective loss of interneurons in experimental epilepsy. Science, 235, 73-76.
50. Sloviter, R. S. (1991). Permanently altered hippocampal structure, excitability, and inhibition after experimental status epilepticus in the rat: The "dormant basket cell" hypothesis and its possible relevance to temporal lobe epilepsy. Hippocampus, 1, 41-66.
51. Sloviter, R. S., Ali-Akbarian, L., Horvath, K. D., & Menkens, K. A. (2001). Substance P receptor expression by inhibitory interneurons of the rat hippocampus: Enhanced detection using improved immunocytochemical methods for the preservation and colocalization of GABA and other neuronal markers. Journal of Comparative Neurology, 430, 283-305
52. Sloviter, R. S., & Nilaver, G. (1987). Immunocytochemical localization of GABA-, cholecystokinin-, vasoactive intestinal polypeptide-, and somatostatin like immunoreactivity in the area dentata and hippocampus of the rat. Journal of Comparative Neurology, 256, 42-60.
53. Sloviter, R. S., Sollas, A. L., Barbaro, N. M., & Laxer, K. D. (1991). Calcium-binding protein (calbindin-D28K) and parvalbumin immunocytochemistry in the normal and epileptic human hippocampus. Journal of Comparative Neurology, 308, 381-396.
54. Sloviter, R. S., Zappone, C. A., Harvey, B.D., Bumanglag, A. V., Bender, R. A., & Frotscher, M. (2003). "Dormant basket cell" hypothesis revisited: Relative vulnerabilities of dentate gyrus mossy cells and inhibitory interneurons after hippocampal status epilepticus in the rat. Journal of Comparative Neurology, 459, 44-76.
55. Sperk, G., Marksteiner, J., Gruber, B., Bellmann, R., Mahata, M., & Ortler, M. (1992). Functional changes in neuropeptide Y- and somatostatin-containing neurons induced by limbic seizures in the rat. Neuroscience, 50, 831-846.
56. Sun, C. S., Mtchedlishvili, Z., Bertram, E. H., Erisir, A., & Kapur, J. (2007). Selective loss of dentate hilar interneurons contributes to reduced synaptic inhibition of granule cells in an electrical stimulation-based animal model of temporal lobe epilepsy. Journal of Comparative Neurology, 500, 876-893.
57. Veliskova, J. (2006). Behavioral characterization of seizures in rats. In A. Pitkanen, P. A. Schwartzkroin & S. L. Moshe (eds.), Models of Seizures and Epilepsy. Burlington, VT: Elsevier Academic Press, 601-611.
58. Vezzani, A., Schwarzer, C. O., & Lothman, E. W. (1996). Functional changes in somatostatin and neuropeptide Y containing neurons in the rat hippocampus in chronic models of fimbic seizures. Epilepsy Research, 26, 267-279.
59. Wittner, L., Eross, L., Szabo, Z., Toth, S., Czirjak, S.,Halasz, P., et al. (2002). Synaptic reorganization of calbindin-positive neurons in the human hippocampal CA1 region in temporal lobe epilepsy. Neuroscience, 115, 961-978.
60. Wittner, L., Maglóczky, Z., Borhegyi, Z., Halász, P., Tóth, S., Eross, L., et al. (2001). Preservation of perisomatic inhibitory input of granule cells in the epileptic human dentate gyrus. Neuroscience, 108, 587-600.
61. Wu, K., & Leung, L. S. (2001). Enhanced but fragile inhibition in the dentate gyrus in vivo in the kainic acid model of temporal lobe epilepsy: A study using current source density analysis. Neuroscience, 104, 379-396.
62. Yang, Z. X., Luan, G.M., Yan, L., & Zhang, Y. (2004). Establishment of temporal epilepsy models and its permanent epilepsy sensitivity. Chinese Medical Journal, 84, 152-155.
63. Zhang, X., Cui, S.-S., Wallace, A. E., Hannesson, D. K., Schmued, L. C., Saucier, D. M., et al. (2002). Relations between brain pathology and temporal lobe epilepsy. Journal of Neuroscience, 22, 6052-6061.